Journal
J Comp Physiol (1982) 147:401-414
Transmission Mediated With and Without Spikes at Connexions
Between Large Second-Order Neurones of Locust Ocelli
Peter J. Simmons
Department of Zoology, University of Newcastle upon Tyne, Newcastle upon Tyne NE1 7RU, England
Accepted February 19, 1982
Summary. Large second-order neurones of locust
ocelli (L-neurones) make both excitatory and inhibi-
tory connexions with each other. Small, graded depo-
larisations and hyperpolarisations are transmitted at
the excitatory connexions but, at the inhibitory con-
nexions, spikes in the presynaptic neurone are re-
quired for transmission.
1. L-neurones spike, usually once only, when hy-
perpolarisations end rapidly. The hyperpolarisations
can be caused either by illumination of the ocellus,
or by injection of current. The amplitude of a spike
depends both upon the amplitude and the duration
of the preceding hyperpolarisation (Fig. 1 B).
2. At the excitatory connexions, the resting poten-
tial of the presynaptic neurone normally lies depolar-
ised from the threshold for transmission, so that both
small hyperpolarisations and depolarisations effect
changes in postsynaptic potential (Fig. 2A, B). Over
periods of several minutes, there is no sign of de-
crement in transmission at these connexions
(Fig. 2D). Spikes in the presynaptic neurone usually
ensure that the postsynaptic neurone also spikes.
3. At the inhibitory connexions, the postsynaptic
potential decrements within 10-20 ms (Fig. 3A). Be-
cause of this, rapidly rising presynaptic potentials,
such as spikes, are required for transmission. Also,
presynaptic hyperpolarisations do not effect changes
in postsynaptic potential. Following an inhibitory
postsynaptic potential, transmission at an inhibitory
connexion remains depressed for about a second
(Figs. 3 B, C).
4. All three members of one anatomical class of
L-neurone (Ll-3; C.S. Goodman 1976) of a lateral
ocellus make reciprocal inhibitory connexions with
each other (Fig. 7B ; Table 1). Some of these neurones
are presynaptic at excitatory connexions with another
class (L4-5; Fig. 7A). Many L-neurones do not pro-
Abbreviation: L-neurone large second-order neurone
of Comparative
Physiology. A
9 Springer-Verlag 1982
ject to the whole area of the retina, and most project
to the dorsal or ventral halves (Fig. 6). The excitatory
connexions may sharpen responsiveness to decreases
in illumination, and the inhibitory connexions may
enhance the detection of rapid movements of large
objects, such as the visual horizon.
Introduction
The reasons why particular neurones should or should
not be able to produce spikes are not always clear.
In some cases spikes are necessary because signals
must travel some distance within a neurone's axon.
However, there are examples where one type of neu-
rone produces spikes, whereas another type, of similar
dimensions does not. For instance, in the vertebrate
retina amacrine cells spike, but horizontal cells -
which are of comparable size to them - do not (Werb-
lin and Dowling 1969); and in the thoracic ganglia
of locusts, the morphologies of local neurones which
normally operate without spikes (Siegler and Burrows
1979) are very similar to those of other local neurones
which produce trains of spikes (M. Burrows and
M.V.S. Siegler, personal communication). For small
neurones, it could be seen as disadvantageous to em-
ploy spikes, as time is required to convert a signal
expressed as spike frequency into one expressed as
membrane potential. In this paper it is shown that
spikes are required for transmi~ssion at one type of
connexion made between large, second-order neu-
rones of locust ocelli. Spikes are required because
the effectiveness of transmission declines very fast,
so that a rapidly rising depolarising signal, such as
a spike, is needed in the presynaptic neurone. These
same second-order neurones also make another type
of connexion amongst themselves where spikes are
0340-7594/82/0147/0401/$02.80
402 P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts
not required for transmission, and at which small
depolarisations or hyperpolarisations in the presyn-
aptic neurone effect changes in postsynaptic potential.
Large second-order neurones of insect ocelli
(called 'L-neurones' in the locust by C.S. Good-
man 1976) hyperpolarise when illumination increases,
and may spike when light intensity decreases rapidly
(Chappell and Dowling 1972 - dragonfly; Patterson
and L.J. Goodman 1974; Wilson 1978a, b - locust;
Guy et al. 1979 - bee). Some of the membrane proper-
ties of L-neurones have been investigated (Wilson
1978b), and the operation of excitatory synapses
which they make with some large brain neurones has
been described (Simmons 1981b). At these synapses,
under ordinary conditions of illumination, transmitter
is continually released, so that both depolarising and
small hyperpolarising changes in presynaptic poten-
tial are communicated to the postsynaptic neurones.
Evidence that L-neurones synapse with each other
has been found before in an ultrastructural study (L.J.
Goodman et al. 1977), where synaptic structures were
found in the ocellar nerve and in the ocellar tracts
in the brain. Ultrastructural studies also suggest the
possibility that L-neurones interact in the ocellar neu-
ropile (Dowling and Chappell 1972 - dragonfly; L.J.
Goodman et al. 1979 - locust).
Materials and Methods
Experiments were performed on male and female Sehistocerca gre-
garia (Forskal), a n d most of the methods used have been described
in more detail before (Simmons 1981 b).
The brain was exposed and stabilised by manipulating a small
platform to lie beneath it. It was constantly bathed in saline at
18-20 ~ In the purely physiological experiments, intracellular
glass capillary electrodes were filled with 2 tool/1 potassium acetate.
Initially electrodes had d.c. resistances of 40-70 M O h m , and this
was often reduced by bevelling to 20-25 M O h m . To stain single
neurones, they were injected with 5% cobalt chloride and later
intensified (Bacon and A l t m a n 1977). W h e n two neurones to the
same oceilus were stained, one was injected with cobalt chloride
and the other with nickel chloride. On reaction with rubeanic
acid, cobalt-filled neurones stained red and nickel-filled neurones
blue (Quieke and Brace 1979). Light was delivered to each ocellus
separately t h r o u g h a plastic light guide (' Crofon', du Pont), a n d
light sources were lens-end torch bulbs, each provided with a me-
chanical shutter. In some experiments stimulus programs applied
to neurones were controlled by a microcomputer.
Particular care was taken to ensure L-neurones were not dam-
aged (criteria in Simmons 1981b). Neurones were identified as
L-neurones purely by the way they responded to pulses of light.
Over 160 neurones identified as L-neurones in this way have subse-
quently been stained, and all have had the structure of an L-
neurone (C.S. G o o d m a n 1976). Most recordings were made from
L-neurone axons, within 200 g m (either side) of where they enter
the brain. Most recordings were made from L-neurones of the
lateral ocelli as, in Schistocerca, the nerves to these ocelli are more
accessible t h a n that of the median ocellus.
Results
Spikes in L-Neurones
Spikes in L-neurones are produced when hyperpolar-
isations, induced either by illumination of photore-
ceptors or, as reported by Wilson (1978b), by injec-
tion of current through a microelectrode, end
abruptly. The amplitude of a spike depends both upon
the amplitude and duration of the preceding hyperpo-
larisation. In Fig. 1A are recordings from an L-neu-
rone, penetrated with two microelectrodes, to three
identical pulses of light delivered during three differ-
ent amplitudes of hyperpolarising pulse injected into
the neurone. As the neurone was more strongly hyper-
polarised, the amplitude of the spike produced at
the end of the pulse of light increased. The hyperpo-
larisation induced by the light pulse decreased slightly
in amplitude as the membrane potential of the L-
neurone moved towards the reversal potential of the
neurone's synapses with photoreceptors (Wilson
1978 b). In Fig. 1 B, the amplitudes of spikes produced
at the end of hyperpolarising pulses of different ampli-
tudes ( + ) or durations (.) are plotted. To study the
effects of varying pulse amplitude, current pulses
600 ms long were injected into it, and to study the
effects of varying pulse duration sufficient current
to hyperpolarise the neurone by 35 mV was injected
in each pulse. The plots show that for each successive
equal increment in pulse amplitude or length, the
increase in spike amplitude declines progressively. In-
creasing the length of the pulse beyond 800 ms had
no further effect on spike amplitude. With increasing
pulse amplitude, the maximum spike amplitude
reached was 23 mV above resting (L-neurones have
resting potentials of about - 30 mV, Simmons 1981).
Depolarising pulses are seldom effective at elicit-
ing spikes in L-neurones. Sometimes, when long depo-
larising pulses were injected (e.g. Fig, 2Aiii), there
was a steep depolarising transient, followed by a
notch, but discrete spikes have never been elicited
by short depolarising pulses. When sine waves are
injected into L-neurones, spikes, when elicited,
usually take off as the potential rises towards resting
(Fig. 1 C). In some neurones of the lobula plate of
the fly, hyperpolarisation also enhances the produc-
tion of spikes (Hengstenberg 1977).
L-neurone spikes originate within the brain rather
than in the ocellar neuropile. This is shown in
Fig. 1 D, where a spike was recorded with one elec-
trode in the brain, and a second electrode in an ocellar
process of the same L-neurone, confirming the con-
clusion reached by Wilson (1978b) using the less di-
rect method of recording spike amplitudes at different
locations.
P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts 403

Pul~e chJra~ton, ml
A B

200 400 600 800

[ I i I I
4-
20hA E ....................... 20, §

9
15. 6 §
Spike
amplitude, §

mV I0_ §
I

5..

I I I I
!0 20 30 40
L~gh~
500me Pulom ampl1~ude, mV +

I" i r'----'l

500ms Im8
Fig. 1A-D. Features of spikes in L-neurones. A. Two electrodes were inserted into this L-neurone, one to inject current (monitored
on the bottom trace) and the other to record potential (top trace). Identical 500 ms long pulses of light were delivered to the ocellus.
When no current was injected into the neurone, the intensity of light was not sufficient to cause a spike (0. When the neurone was
hyperpolarised by 7 mV (i/) it produced a spike at the end of the light pulse, End the amplitude of the spike grew as progressively
greater currents were injected (iii). B The effects on the amplitudes of spikes in an L-neurone, produced at the ends of hyperpolarising
current pulses, of varying the amplitude (+) or duration (.) of the pulses. Two electrodes were again used, positioned about 200 gm
apart at the base of the ocellar nerve. C A sinusoidal current was injected into the same neurone that was used for the plots in
B. Initially the neurone was at its normal resting potential, and a spike took off at a potential more negative than this during repolarisation
following hyperpolarisation. No spike was produced when the neurone was initially depolarised. D L-neurone spikes travel away from
the brain. This spike occurred at the end of a pulse of light. The electrode for the upper trace was placed in the ocellar tract in
the brain, and that for the lower was placed in the ocellar neuropile

The Excitatory Connexions n e u r o n e s synapse with each other over a c o n s i d e r a b l e

The o p e r a t i o n of excitatory c o n n e x i o n s between L-
n e u r o n e s has been studied in detail in 6 different prep-
arations, a n d m o r e cursorily in a b o u t 25. T h e results
presented here are representative of all of these. The
excitatory c o n n e x i o n s operate in a n identical m a n n e r
to the excitatory c o n n e x i o n s which L - n e u r o n e s m a k e
with the large descending n e u r o n e s 03 a n d 04 (Sim-
m o n s 1981 b).
The length c o n s t a n t of a n L - n e u r o n e is m u c h lon-
ger t h a n the length of the n e u r o n e itself ( W i l s o n
1978b; c o n f i r m e d by p e r s o n a l observations). This
m e a n s that p o t e n t i a l s recorded f r o m a n L - n e u r o n e
a x o n at the p o i n t were it enters the b r a i n - which
was the u s u a l site for p o s i t i o n i n g electrodes - will
be very similar to those o c c u r r i n g elsewhere in the
n e u r o n e . L.J. G o o d m a n et al. (1977) report that L-
part o f the ocellar tract within the brain, as well
as in the nerve itself, so t h a t p o t e n t i a l changes re-
corded in the present work are p r o b a b l y those which
actually occur at the presynaptic sites.
The o p e r a t i o n o f a n excitatory c o n n e x i o n in one
p r e p a r a t i o n is described by Fig. 2. T w o electrodes
were inserted into the p r e s y n a p t i c n e u r o n e , one to
inject c u r r e n t a n d the other to record p o t e n t i a l
changes (the results were a l m o s t identical w h e n the
roles of the two electrodes were reversed). A third
electrode recorded the m e m b r a n e p o t e n t i a l of the
p o s t s y n a p t i c n e u r o n e . T o study the transfer of sus-
t a i n e d graded potentials across the c o n n e x i o n ,
500 m s - l o n g pulses of c u r r e n t were applied to the
presynaptic n e u r o n e (Fig. 2A). The a m p l i t u d e o f the
presynaptic p o t e n t i a l at the middle o f each pulse is
plotted against the c o r r e s p o n d i n g p o s t s y n a p t i c p o t e n -
404 P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts

A B

5mV
~OmV Po8s s
m
II

20~A mV 4
m

Currens 3
2 R ~

1 m

. ' I I I I I I I
-40 -30 -20 -lg i0 20 30 40
-i
w
%
-2 Pre- mV
9 q 9 9

ii
-3

i ii

iV 5mV

. . . . . . . . . . ~

50mV
500ms puJ-ses
5mR

mV [ 2mV

~o v 9 f............ ........... = ' L .............

20,~^ ~ ......
r---n 1 sec
1 ms

Fig. 2 A - E . The operation of an excitatory connexion between two L-neurones. In all records two electrodes were inserted into the
presynaptic neurone, one to inject current and the other to record potential. Records are all from the same pair of nenrones. Records
from the postsynaptic neurone on the top trace, with records from the presynaptic neurone below them. A (i) A depolarising pulse
was applied to the presynaptic neurone. A small spike leads the more sustained potential and the postsynaptic neurone also spiked at
the beginning of the pulse. (ii-iv) progressively larger hyperpolarising pulses were injected into the presynaptic neurone. B A plot of
presynaptic against postsynaptic potentials, made from an enlarged series of records, including those in A. C A comparison of an EPSP
elicited by a presynaptic spike (/) with one elicited by a depolarising pulse (i0. The postsynaptic neurone was depolarised by 5 n A
to reduce its tendency to spike (one electrode was used to inject current a n d record from this neurone). Dotted lines: n o r m a l presynaptic
resting potential. In (i/) there was an initial transient peak in the presynaptic neurone when the depolarising pulse was applied, right
at the start of this sweep. D M e a s u r e m e n t of transmission latency across the connexion. Depolarising pulses were injected into the
presynaptic neurone, and 5 single sweeps are superimposed. E A 5 min long depolarising pulse was applied to the presynaptic neurone;
start and end of this pulse are shown.

tial in Fig. 2 B. The plot shows that the normal resting
potential of the presynaptic neurone lies 14 mV depo-
larised from the threshold for transmission, so that
both positive and negative potential changes in the
presynaptic neurone effect potential changes in the
postsynaptic neurone. For presynaptic potentials be-
tween 10 mV below and 20 mV above resting, each
1 mV change in presynaptic potential caused a change
of 0.27 mV in postsynaptic potential.
Usually at excitatory connexions, spikes in the
presynaptic neurone would always drive the postsyn-
aptic neurone to spike (Fig. 2A). This meant that
it was difficult to compare the amplitudes of postsyn-
aptic potentials produced by presynaptic spikes with
those produced by more sustained presynaptic depo-
larisations. In a few preparations, the postsynaptic
neurone was reluctant to spike, and this comparison
could be made. Alternatively, small depolarising cur-
rents applied to the postsynaptic neurone would
sometimes block spikes in it. In Fig. 1 C a steady
current of + 5 nA was injected into the postsynaptic
neurone, and this reduced its tendency to spike. A
spike was produced in the presynaptic neurone at
the end of a hyperpolarising pulse applied to it, and
P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts 405

A i B
g
I
5mY [ Ampii~udm 8O
50mY
o~ 2rid 8O
ii IPSP ag 4O m

% o~ le~. 2O
200 400 800 800 IOOO
| |
I I I I 1 1 I I I I

Interval 6es ~plkee, me

C i ii iii

5mY

50mY
200hA

200ms
D

&

lOm~
Fig. 3A-D. Decrement and recovery from depression of transmission at inhibitory connexions. Records from postsynaptic neurones
are on all upper traces, and from presynaptic neurones on second traces. In A and C separate electrodes were used for injecting
current into and recording from the presynaptic neurones. A Comparison between IPSPs elicited by a presynaptic spike (0 and by
a longer depolarising pulse (ii). In both cases the IPSP decrements within 10 ms, although the presynaptic neurone remained depolarised
throughout the length of the pulse in (i0. The spike in (0 was elicited at the end of a 500 ms long hyperpolarising pulse. B, C Recovery
of transmission from depression. Pairs of spikes were elicited in the presynaptic neurone, each elicited by a brief hyperpolarising pulse
(current monitored on bottom trace). The interval between the spikes was varied (C i-iii), and the amplitudes of the IPSPs were measured.
In B five repetitions of each interspike interval were used to plot each point. D Recordings from 3 separate L-neurones, which all
made reciprocal inhibitory connexions with each other. Spikes were elicited in two of them (bottom two traces), eliciting IPSPs in
the third (top trace). Although the spikes were separated by only 25 ms, the amplitude of the second IPSP was not diminished by
the occurrence of the first. In each presynaptic neurone, a single electrode passed current and recorded potential, and the bridge
circuits of the DC amplifiers used were approximately balanced

was followed by a n excitatory p o s t s y n a p t i c p o t e n t i a l
(EPSP) in the p o s t s y n a p t i c n e u r o n e (Fig. 2 Ci). W h e n
a pulse of c u r r e n t was injected into the presynaptic
n e u r o n e to depolarise it to the same p o t e n t i a l as that
reached by the spike, the a m p l i t u d e of the E P S P was
i n d i s t i n g u i s h a b l e f r o m that p r o d u c e d by tile spike
(Fig. 2 Cii).
The latency for t r a n s m i s s i o n was m e a s u r e d by ap-
plying depolarising pulses to the presynaptic n e u r o n e ,
so that there was n o extra time required for the pre-
synaptic n e u r o n e to exceed a threshold for t r a n s m i t t e r
release. F o r this c o n n e x i o n it was a b o u t 2 m s
(Fig. 2D). A t some others it was u p to 2.5 ms, b u t
it is often difficult to j u d g e the p o i n t at which post-
synaptic p o t e n t i a l first begins to change.
N o sign of d e c r e m e n t in the E P S P was f o u n d
when very long depolarising pulses were injected into
the presynaptic n e u r o n e . Such a pulse 5 m i n long
406 P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts

A Spike amp., mV.

-I0 0 I0 20
,
! u u u B

IPSP I

I
Im

mV
-2

-3 i

ii

-4

iii

c D

E [
5mY [ 20mY
9 9 9 . 9 ~ 9 9

lOm~
Fig. 4A-D. Transmission characteristics of an inhibitory connexion between two L-neurones. A, B The presynaptic neurone (middle
traces) was injected with current to hyperpolarise it to 15 mV below resting, and pulses of additional hyperpolarising current (lower
traces) elicited spikes in it. Separate electrodes were used to inject current and record potential. Each spike elicited an IPSP in the
postsynaptic neurone (top traces). Note that in (z) the spike reaches an amplitude which is negative from the normal resting potential.
Spikes of this amplitude were only rarely produced, and so plots of transmission characteristics of these connexions are not detailed
for smaller presynaptic potentials, and it is not possible to arrive at estimates of thresholds for transmission. In (i0 and (ii~) are
progressively larger spikes. Note that here the IPSPs lasted about twice as long as those in Fig. 3A. Calibrations: presynaptic, 20 mV;
postsynaptic, 1 mV; current, 40 nA; 50 ms. B Plot of spike amplitude, relative to the normal resting potential, against IPSP amplitude.
C Estimate of transmission latency. Five different spikes were elicited in the presynaptic neurone. The difficulty in measuring latency
is to know which pre- and postsynaptic potentials to take. The shortest estimate is 3.7 ms, between the point where the smallest
spike starts to rise sharply, and where a negative inflexion is first seen in the postsynaptic recording (recording on the right). D In
this preparation, IPSPs could be seen to travel away from the brain. One electrode injected current into the presynaptic neurone
and recorded spikes in it (lower trace) while one electrode recorded from the postsynaptic neurone near the base of the ocellar nerve
(middle trace) and a third recorded the IPSPs in the ocellus (top trace). Four sweeps superimposed

was a p p l i e d in t h e r e c o r d i n g f r o m w h i c h Fig. 2 D is p r e s s e d for a b o u t a s e c o n d (Fig. 3). I n Fig. 3 Ai, t h e

t a k e n . N o d o u b t if l o n g e r p u l s e s o r m o r e i n t e n s e
d e p o l a r i s a t i o n s w e r e a p p l i e d , signs o f E P S P d e -
c r e m e n t w o u l d a p p e a r , b u t it also b e c o m e s h a r d e r
to m a i n t a i n s t a b l e r e c o r d i n g s .
The Inhibitory Connexions
T r a n s m i s s i o n at i n h i b i t o r y c o n n e x i o n s b e t w e e n L-
n e u r o n e s d e c r e m e n t s v e r y r a p i d l y , a n d r e m a i n s de-
p r e s y n a p t i c n e u r o n e s p i k e d at t h e e n d o f a h y p e r p o -
l a r i s i n g p u l s e w h i c h was i n j e c t e d i n t o it, a n d a n i n h i b i -
t o r y p o s t s y n a p t i c p o t e n t i a l ( I P S P ) f o l l o w e d i n the
p o s t s y n a p t i c n e u r o n e . T h e d u r a t i o n o f the I P S P was
a b o u t 10 ms. W h e n a 40 m s l o n g p u l s e o f d e p o l a r i s i n g
c u r r e n t was i n j e c t e d i n t o the p r e s y n a p t i c n e u r o n e
(Fig. 3Aii), the d u r a t i o n o f the I P S P was n o l o n g e r
t h a n t h a t f o l l o w i n g a spike. I n a d d i t i o n , a l t h o u g h
the a m p l i t u d e o f the d e p o l a r i s i n g p u l s e in Fig. 3 A i i
was g r e a t e r t h a n t h a t o f t h e spike i n Fig. 3 Ai, the
P.J. Simmons: Connexions Between Second-Order Oce1Iar Neurones of Locusts
amplitude of the IPSP was no greater. This is because,
preceding the depolarising pulse, the presynaptic neu-
rone was at its normal resting potential, which has
the effect of depressing transmission (see below). In
all cases where transmission at inhibitory connexions
has been examined (8 cases in detail, with two elec-
trodes in the presynaptic neurone, and over 50 cases
more cursorily, with only one electrode in the presyn-
aptic neurone), IPSPs have decremented very rapidly:
usually within 10 ms, and have never been found to
last more than 20 ms.
To plot the recovery of transmission at an inhibi-
tory connexion following its depression caused by
a single presynaptic spike, pairs of sp!kes, separated
by a variable interval, were induced in the presynaptic
neurone by injecting short hyperpolarising pulses into
it (Fig. 3 C). In the plot of Fig. 3 B, for each spike
separation interval, the amplitude of the second IPSP
is expressed as a percentage of the first. The IPSP
recovered to 50% of its original amplitude in 225 ms,
and recovered completely in about 1 s. Two other
experiments on different preparations revealed very
similar time courses for recovery from depression.
Many L-neurones receive IPSPs from connexions
with at least two other L-neurones (see results on
L-neurone interconnectivity). An IPSP mediated by
one connexion does not appear to depress transmis-
sion at another connexion (Fig. 3 D).
In experiments to plot the relationship between
presynaptic and postsynaptic potential changes at in-
hibitory connexions, the presynaptic neurone was
held at a potential about 15 mV hyperpolarised from
resting. This potential is below the threshold for trans-
mission at the excitatory connexions (Fig. 2B), and
so it is also likely that no transmission, and therefore
no depression of transmission, would occur at the
inhibitory connexion under study when the presyn-
aptic neurone was held hyperpolarised by this
amount. The results of one experiment, which are
representative of the other two successfully per-
formed, are shown in Fig. 4A and B. In the records
of Fig. 4A, short hyperpolarising pulses were applied
to the presynaptic neurone, which was already held
hyperpolarised by 15 mV, to induce spikes in it. The
plot in Fig. 4B was made from a series of similar
recordings, and also a series where 50 ms long depo-
larising pulses were applied instead of the hyperpolar-
ising ones. For presynaptic spikes reaching ampli-
tudes between resting potential and 40 mV above it
(the maximum reached), each 1 mV increase in pre-
synaptic potential causes an increase of about 0.1 mV
in IPSP amplitude. The plot shows that depolarising
potentials which jump from the - 15 mV holding po-
tential to potentials more negative than resting can
effect transmission. This Was usually difficult to dem-
407
A B
50mY- -- 40mV~"--~ ~ - - ~
-4OrnV
40mY [ ~ -50rnV I"
l__.__l
IOtas
Fig. 5A, B. Reversal of EPSPs (A) and IPSPs (B). In each case
one electrode passed current into and recorded spikes from the
presynaptic neurone (lower traces). In the postsynaptic neurones,
separate electrodes recorded potential and injected current.
A The postsynaptic potential follows presyuaptic potential as the
presynaptic neurone is released from a hyperpolarising pulse and
then spikes. The polarity of the postsynaptic response reversed
when the neurone was depolarised by more than 45 mV from resting.
B Reversal o f an IPSP at 45 mV negative from resting
onstrate directly because it was difficult to produce
suitable presynaptic potential changes - spikes usually
boosted membrane potential well over resting poten-
tial. Some attempts to employ a voltage clamp, allow-
ing presynaptic potential to be controlled more direct-
ly, were made, but caused unacceptable stimulus arte-
facts.
The latencies of IPSPs at these connexions are
greater than those of EPSPs at the excitatory connex-
ions. Measurement of latency is difficult because,
since the IPSPs are depressed if the presynaptic ter-
minal is depolarised, it is difficult to decide at what
presynaptic potential to start measurement of the de-
lay before the first sign of the IPSP. In Fig. 4B, spikes
of different amplitudes in the presynaptic neurone
were induced at the ends of various hyperpolarising
pulses. For the largest presynaptic spikes, there is
a delay of 5 ms before the postsynaptic potential starts
to hyperpolarise sharply. This may overestimate the
delay, since, in some traces, it can be seen that the
postsynaptic neurone starts to hyperpolarise sooner
than this. For instance, the delay between the inflex-
ion where the smallest spike begins to rise and the
point at which the corresponding hyperpolarisation
of the postsynaptic neurone is first detectable is
3.7 ms. The shortest measurements of latencies at the
inhibitory connexions was 3.5 ms, and this will be
taken as a minimum value for the latency.
Although their amplitude is rather small, IPSPs
mediated at these connexions appear to reach all parts
of an L-neurone. In Fig. 4D, one electrode was placed
in an L-neurone near the ocellus, and a second elec-
trode in the same L-neurone near to where its axon
408 P.J. Simmons : Connexions Between Second-Order Ocellar Neurones of Locusts

Pig. 6A-C. Three different lateral ocelli in which single L-neurones have been stained with cobalt and intensified. The base of an
antenna can be seen at the bottom of each ocellus. The ocelli are photographed from within the head capsule; nerves have been
cut. A An L-neurone L4-5 (see text) which projected to the dorsal part of the retina. This was neurone 1 of Fig. 7A. B Another
neurone Lz~5 projected to the ventral half of this ocellar retina. C This neurone of class L1-3 projected to all parts of the retina.
Most other fills of L1-3 neurones have revealed more restricted projections. Bar in A 100 gm

enters the brain. A third electrode was used to inject
current into and record from another L-neurone,
which made an inhibitory connexion with the first.
IPSPs mediated by spikes in the second L-neurone
were recorded by the proximal electrode before the
distal one, showing that they originate in the brain
(or in a proximal region of the ocellar nerve) rather
than in the ocellus. On one other occasion, IPSPs
could be shown to travel away from the brain, and
they have never been recorded travelling towards it.
Reversal Potentials of EPSPs and IPSPs
Reversal potentials of EPSPs and IPSPs were mea-
sured by employing one electrode in a postsynaptic
L-neurone to inject 500 ms long pulses of current
into it; a second electrode to monitor postsynaptic
potential; and a third electrode both to pass current
into and record from the presynaptic neurone.
Results from one experiment with an excitatory
connexion are shown in Fig. 5A, and results from
another experiment, with an inhibitory connexion,
in Fig. 5 B. Five measurements of EPSP reversal were
made in different animals and gave a mean value
of 45 mV above resting (range 22 mV to 65 mV; L-
neurone resting potential is about - 30 mV, Simmons
1981). For IPSPs, five different preparations gave a
mean of 50 mV negative from resting (range 40 mV
to 60 mV). These measurements show that both the
EPSPs and IPSPs are generated by an increased per-
meability to one or more species of ion.
The Pattern of L-Neurone Interconnectivity
Three separate anatomical classes of L-neurone con-
nect each lateral ocellus with the brain (C.S. Good-
man 1974) and in this account they are named after
the terminology of C.S. G o o d m a n (1976). Two neu-
rones, MLI22, connect the median ocellus with a
lateral, and do not branch in the brain except for
a narrow neurite to the cell body. The remaining
two groups project only to the lateral ocellus and
are distinguishable by the length of their projection
in the brain, L4-5 projecting further towards the trito-
cerebrum than L1-3, and by the positions of their
cell bodies. In order to establish the identities of the
lateral ocellar L-neurones which make the different
types of connexion, and so to determine a wiring
pattern, pairs of L-neurones were penetrated, the type
of connexion between them established, and then the
neurones were stained. One neurone was injected with
cobalt and the other with nickel so that they could
later be distinguished (Quicke and Brace 1979). In
addition, several single L-neurones have been stained,
following study of some of their connexions. Most
of these single neurones were intensified. In about
half of the preparations, details of an L-neurone's
projection to the retina were revealed. Three different
types of projection to the ocellar neuropile are shown
in Fig. 6. Usually L-neurones seem to project either
to the dorsal (Fig. 6A) or ventral (Fig. 6B) half but
some project to the anterior or posterior (towards
the compound eye). Three L l - 3 neurones have been
P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts 409

Table 1. Interconnexions of identified L-neurones. ? indicates that ML1-2, which respond to illumination of the median
the neurone was not stained sufficiently to permit identification
as well as the lateral ocellus; and third, L4-5 have
Identity of neurones Number
never been stained when reciprocal inhibitory connex-
of preparations ions have been found. The second generalisation is
that members of L1-3 excite one or both of L4-5.
1. Excitatory connexions Most excitatory connexions encountered were of this
Pre- L1-3 : post- L4-5 9 type (Table 1). In Fig. 7A are recordings from a pair
Pre- L4-5: post- L4-5 1 of mutually-inhibitory L-neurones ( L l - 3 by the first
Pre- MLI~: post- L4-5 1
generalisation) which each excited a third L-neurone.
Pre- L1-3 : post- ? 1
Pre- ML1 2: post- ? 1 This third neurone was stained and found to be of
Pre- ?: post- L4-5 3 the pair L4-5, and to project to the top half of the
2. Inhibitory connexions
retina (the neurone of Fig. 6A). The combination of
one L-neurone which excites two different postsynap-
One-way:
Pre- L1 3 : post- L4-5 1 tic L-neurones has never been found, which suggests
Pre- ML1-2: post ? 1 that both L4 and L-5 are not excited by the same
Reciprocal: neurones. A third possible generalisation is that ML1
L1-3 : L1 3 14 makes a reciprocal inhibitory connexion with ML2,
MLI~: ML1-2 4 but this only relies on 4 preparations (Table 1). F r o m
LI-3: ? 4 the records of pairs of neurones recorded from at
3. No connexion found the bottom of Table 1 it can be seen that far fewer
L4-5 : L4-5 3 M L I - 2 neurones have been stained than the other
ML1-2 : L4-5 1 two categories. The reason for this is that they appear
LI-3 : L4-5 2 to make fewer connexions than the other two types,
LM1-2:" ? 2
and that when no connexion could be f o u n d between
Totals of pairs recorded two L-neurones, one electrode was usually withdrawn
Ll-3 : L1 3 14 (all inhibitory) and placed in another L-neurone rather than staining
L1 3 : L4-5 12 (9 excitatory) the original two L-neurones.
LI-3 : ML1-2 0 Details of the connectivity pattern of L-neurones
L4-5: L4-5 4 (3 no conn.)
L4 5: ML1-2 2
might vary from one locust to another. One example
MLI-2: ML1-2 2 of this, from Table 1, is that an excitatory connexion
Total: 34 between one of the L4-5 pair and the other was found
on one occasion, but on four other occasions when
a These neurones were not stained, but identified by illuminating
this pair was stained no connexion was found. A
the different ocelli
second example is that a one-way inhibitory connex-
ion from an L1-3 neurone to one of L4-5 was found
in one preparation, and this was exceptional. It is
not to be unexpected that variation in the connectivity
stained with projections to all parts of the retina pattern should occur, since variation in L-neurone
(Fig. 6C). Some L-neurones project to only about structure is well documented (C.S. G o o d m a n 1978),
one third of the ocellar retina. It may be that individ- and variation in connectivity of identified neurones
uals of each sub-class can be uniquely identified by in locusts has been reported previously (Pearson and
their projection to the retina. C.S. G o o d m a n 1979).
The results of 34 experiments where pairs of L- No obvious correlation between the way two L-
neurones have been penetrated and later identified neurones were connected and their projections to the
anatomically are given in Table 1. Also, in a number retina emerged (Table 2), but the sample obtained
of experiments, three different L-neurones have been is small.
penetrated simultaneously, and the nature of connex- In Fig. 8 are shown recordings from a succession
ions between them studied (usually none of these were of pairs of L-neurones together with 03, a large de-
stained). Results of two such experiments are shown scending brain neurone. L-neurones make excitatory
in Fig. 7. Two generalisations can be made. The first connexions with 03 (Simmons 1981b) which operate
is that each of the three L-neurones L1 3 makes a like those they make amongst themselves. The gener-
reciprocal inhibitory connexion with the other two. alisations presented above provide evidence for an
The argument in support of this is: first, three differ- anatomical identity for the L-neurones recorded from
ent L-neurones interconnected in this way were found in Fig. 8, and lead to the conclusion that members
in five different preparations (Fig. 7B is one exam- of all three anatomical group drive it. Figure 8 C
ple); second, the neurones involved did not include shows that when one L-neurone was depolarised by
410 P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts

A g ,~
V

) iv

iv

1
Fig. 7A, B. Two patterns of interconnectivity among L-neurones of a lateral oceilus. A single eIectrode, connected to an amplifier
with a bridge circuit, was inserted in each neurone. A Two neurones, 2 and 3, inhibited each other and each excited a third neurone
1. This is shown in the connectivity diagram (v). In this diagram, triangles with+symbols indicate excitatory connexions and filled
circles with - symbols indicate inhibitory connexions. The numbers of the neurones correspond to the order of the traces in the
records. Hyperpolarising pulses were injected into each neurone in turn, causing it to spike, and dots indicate which neurone is being
driven to spike in each record. In (iii) the spike is mis-shapen because the electrode resistance was not linear, so that the bridge
imbalance varied. In (iv) insufficient current was injected into neurone 3 to elicit a spike in it. Its excitatory connexion with neurone 1
operates, but no sign of an IPSP in neurone 2 is apparent. Neurone 1 was stained and found to belong to class L4-5. Results presented
in Table 1 suggest that 2 and 3 belonged to class 1-3. None of these neurones responded to illumination of the median ocellus.
Calibrations: 10 ms; neurones induced to spike, and 3 in 4, 20 mV; neuron 1 EPSPs, 5 mV; traces with IPSPs, 2 inV. B Three L-neurones
which make reciprocal inhibitory connexions with each other. Connectivity pattern is drawn in (iv). In (i-iii) each neurone in turn
was induced to spike (dots), and IPSPs recorded from the other two. None of these neurones responded to illumination of the median
ocellus, and they were probably the neurones L1-3. Calibrations. 5 mV; neurones with spikes, 30 mV; neurones with IPSPs, 5 mV

Table 2. Ocellar projections of pairs of lateral L-neurones. ? indi- t h e l a t e r a l a n d m e d i a n ocelli, b u t t h a t a n o t h e r L-

cates the neurone was not filled sufficiently to allow identification
n e u r o n e ( L 1 - 3 ) r e s p o n d e d o n l y to i l l u m i n a t i o n o f t h e
Projections No. of Neurone identity l a t e r a l ocellus. ( N o t e t h a t since, as T a b l e 1 s h o w s ,
preparations M L I - 2 c a n excite L 4 - 5 t h e n L 4 - 5 c a n also r e s p o n d
to i l l u m i n a t i o n o f t h e m e d i a n ocellus).
1. Excitatory connexions
Dorsal: ventral 2 Pre- L1-3 : post- L4-5
Posterior: posterior 1 ?: ?
Discussion
2. Inhibitory connexions (all reciprocal)
Dorsal: ventral 4 Synaptic Transmission
Posterior: posterior 1 All
M e d i a t e d with and without S p i k e s
Dorsal: dorsal 1 L1-3
Anterior: ventral 1 The connexions between L-neurones are remarkable
3. No connexion found because of the difference between the tonic nature
Dorsal: ventral 2 ?: ? o f t r a n s m i s s i o n at t h e e x c i t a t o r y c o n n e x i o n s a n d t h e
Posterior: dorsal 1 MLI-2 (back): ? p h a s i c n a t u r e o f t r a n s m i s s i o n at t h e i n h i b i t o r y ones.
At some inter-neuronal connexions which have been
s t u d i e d p r e v i o u s l y , t r a n s m i s s i o n is m a i n t a i n e d t o n i -
cally w h e n l o n g d e p o l a r i s a t i o n s a r e i n j e c t e d i n t o t h e
i n j e c t i o n o f 10 n A ( w h i c h w o u l d p r o b a b l y d e p o l a r i s e p r e - s y n a p t i c n e u r o n e , w h e r e a s at o t h e r c o n n e x i o n s
it b y r a t h e r less t h a n 10 m V a b o v e r e s t i n g ; see W i l s o n t r a n s m i s s i o n is m o r e phasic. T h i s is t h e first e x a m p l e
1978b), this w a s s u f f i c i e n t t o d r i v e s o m e s p i k e s in where both tonically and phasically transmitting con-
03, b u t n o t to p r o d u c e a n I P S P in a n L - n e u r o n e w h i c h n e x i o n s h a v e b e e n f o u n d w i t h a single n e u r o n e as
h a d b e e n s h o w n to be c o n n e c t e d w i t h it (Figs. 8 A the p r e s y n a p t i c e l e m e n t . E x a m p l e s o f t o n i c a l l y t r a n s -
v, vi). I n Fig. 8 D it is s h o w n t h a t o n e L - n e u r o n e m i t t i n g c o n n e x i o n s are t h o s e m a d e b y n o n - s p i k i n g ,
( M L 1 - 2 ) a n d 03 r e s p o n d e d to i l l u m i n a t i o n o f b o t h l o c a l i n t e r n e u r o n e s w i t h m o t o n e u r o n e s in l o c u s t t h o -
P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts 411

i A

1
3

iv

D i ii

C
O3
[ 1 J- ;;%
500me 4 4
j.

LeF~ Median
Fig. 8 A - D . Connexions a m o n g 5 lateral L-neurones and their connexions with 03, a Iarge descending brain neurone. The connectivity
pattern is summarised in B, a n d records providing evidence for it are presented in A. One electrode recorded from 03 continually,
while another two recorded from and injected current into two L-neurones. Neurone 1 was held for the longest, and connexions it
makes with neurones 2, 3 and 4 were studied. After neurone 1 was lost, the electrode was inserted into neurone 5. The connectivity
pattern summarises only those connexions which were found in this preparation - several other connexions m a y have existed. In
each pair of records (i-iv) one neurone was injected with current in the record on the left, the other L-neurone was injected in the
record on the right. Which neurone was injected is indicated with a dot. Calibrations." 10 m s ; 03, 10 m V ; traces with spikes, 20 m V ;
EPSP in (i), 10 m V ; traces with IPSPs, or no PSPs visible, 5 mV. C A small depolarising pulse of 5 n A (bottom trace) was injected
to neurone 1. This elicited a depolarisation and two spikes in 03, but was insufficient to mediate a detectable IPSP in neurone 4.
Calibrations. 03, 5 m V ; 1, 20 m V ; 4, 5 mV. D Responses of 03, neurone 1, and neurone 4 to illumination of the left (i) and median
(ii) ocelli. Pulses of light 500 ms. Neurone 4 gave large responses to illumination of either ocellus, suggesting it was one of the M L 1 - 2
neurones. 03 also responded to illumination of either ocellus, but neurone 1 responded to the left ocellus only. Calibrations: 03, 20 m V ;
1, 4, 40 mV. Probable identities of L-neurones: 1, L1-3; 2, L4-5; 3, L1-3; 4, ML1-2, 5 cannot be identified

racic ganglia (Burrows and Siegler 1978) and by the
'non-impulsive' coxal stretch receptors in crabs with
leg motoneurones (Blight and Llingts 1980). In con-
trast, at excitatory synapses between giant neurones
in the squid (e.g. Katz and Miledi 1967, 1971) and
at some inhibitory synapses in the stomatogastric gan-
glion of the spiny lobster (Graubard 1978), postsynap-
tic potentials climb to an initial peak and then decline
to a more sustained plateau when long depolarising
pulses are applied to the presynaptic terminal. The
transitory IPSP which is found at the inhibitory con-
nexions which L-neurones make amongst themselves
resembles the initial peak of the PSP at the squid
giant synapse (e.g. Katz and Miledi 1971; Kusano
412 P.J. Simmons: ConnexionsBetweenSecond-OrderOcellar Neurones of Locusts
and Landau 1975) and at some stomatogastric gangli-
on synapses (Graubard 1978) in that its amplitude
becomes depressed with repetition and then recovers.
Both depression and recovery occur a little more rap-
idly at the connexions between L-neurones than at
the other two examples. No sign of a sustained pla-
teau response following the initial peak has been seen
at the inhibitory connexions among L-neurones.
Since transmission at the inhibitory connexions
between L-neurones becomes depressed very rapidly,
transmission could decrement during slowly rising
presynaptic potential changes, and the size of the
IPSP will depend on the rate of presynaptic depolar-
isation as well as on its amplitude. Depolarising po-
tentials which rise more slowly than spikes could be
ineffective at mediating IPSPs since the IPSPs de-
crement completely within 10-20 ms (Fig. 3A). The
signal which ocellar photoreceptors produce when il-
lumination is reduced is usually a very slow repolar-
isation from light-induced depolarisation (Patterson
and L.J. Goodman 1974) and this, when inverted
at the synapse with an L-neurone, would be insuffi-
cient to drive the IPSPs. Two further consequences
of the rapid decrement of the IPSPs are: first, in
contrast to the excitatory connexions, at the inhibito-
ry connexions hyperpolarisations of the presynaptic
terminal are ineffective at producing changes in post-
synaptic potential; and second, the amplitude of an
IPSP depends on the recent history of presynaptic
potential change.
There are a number of possible mechanisms for
the rapid depression and subsequent recovery of
transmission at the inhibitory synapses. Presynaptic
mechanisms include a depletion of transmitter avail-
able for release (e.g. Elmqvist and Quastel 1965; Ku-
sano and Landau 1975), and a possible postsynaptic
mechanisms is desensitization (Katz and Thesleff
1957).
The conclusion that one function of spikes in L-
neurones is to enable the rapidly decrementing inhibi-
tory connexions to operate may be applicable to a
number of other inter-neuronal connexions. The most
obvious examples are those involving neurones which
give similar waveforms to those exhibited by L-neu-
rones in response to stimulation. Large monopolar
cells of insect compound eyes (e.g. Shaw 1968; Au-
trum et al. 1970; Laughlin 1973; Lauglin and Hardie
1978) and some amacrine cells of the vertebrate retina
(review, Miller 1979) hyperpolarise when their photo-
receptors are illuminated and generate spikes of vari-
able amplitude when illumination decreases rapidly.
Some of the connexions which these neurones make
may operate in a similar way to the inhibitory connex-
ions made amongst L-neurones, requiring rapid depo-
larising potentials at the presynaptic terminals to en-
sure transmission. Similarly a function of the regener-
ative potentials which have been described in some
neurones which do not generate discrete spikes (e.g.
Blight and Llin/ts 1980; Mirolli 1981 - crab coxal
stretch receptor; Hengstenberg, 1 9 7 7 - lobula plate
neurones in flies) may be to ensure effective transmis-
sion at connexions where PSPs decrement rapidly.
Are the Connexions Monosynaptic ?
Although the latency of transmission at both the ex-
citatory and inhibitory connexions is rather long,
there is anatomical evidence that both types of con-
nexion are monosynaptic (see Maynard and Walton
1975; Graubard 1978; Patterson and Goodman 1974;
Chappell and Dowling 1972 for longer latencies at
presumed monosynaptic connexions). In their ultra-
structural study, L.J. Goodman and co-workers
(1977) found evidence that locust L-neurones synapse
directly with each other in the brain. They also report
that many of the synapses they found were reciprocal.
Since the only reciprocal connexions found in the
present study were inhibitory, whereas all excitatory
connexions were one-way, this is evidence that both
types of connexion are monosynaptic, although the
inhibitory connexions had consistently longer laten-
cies than the excitatory ones.
The conclusions reached above about the role of
spikes in the connexions between L-neurones are not
dependent upon their monosynaptic or polysynaptic
nature. If the connexions can be shown conclusively
to be monosynaptic then a single presynaptic neurone
may make output synapses which have different tem-
poral properties, and may even have different mecha-
nisms controlling the rate of release of transmitter.
Functional Consequences
of the Connexions Among L-Neurones
Any discussion about the contributions that the con-
nexions among L-neurones make to the function of
an ocellus must be speculative until we know more
about the neurones downstream from L-neurones and
the types of stimuli which these higher-order neurones
react to. One implication of the connexions is that
individual L-neurones may have different sensitivities
to various visual stimuli since, as discussed below,
the connexions may enhance differences in the reac-
tions of various L-neurones to stimulation. The dem-
onstration that many L-neurones have projections re-
stricted to one part of the ocellar retina (Fig. 6) also
suggests that L-neurones may differ in their receptive
fields. Previously, L.J. Goodman et al. (1979) and
Taylor (1981a) have reported that L-neurone arbor-
isations do not always extend over the whole ocellar
P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts
retina field, but have not related this to the orientation
of the ocelli. Asymmetry of lateral ocellar L-neurone
projections is particularly marked about the horizon-
tal axis, and this could be an adaptation for sensitivity
to movements of the visual horizon. Wilson (1978a)
has pointed out that L-neurones are particularly well
adapted to monitor movements of the visual horizon,
and that these could be used to stabilise the flight
of an insect. Evidence for this is provided in locusts
by the demonstration that 03, one of the large de-
scending brain neurones which is driven by changes
in ocellar illumination and by wind currents, makes
direct connexions with some flight motoneurones
(Simmons 1980) and by repeatable changes in myo-
grams recorded from tethered flying locusts when
ocellar illumination is altered (Taylor 1981 b). In fly-
ing dragonflies, head movements can be elicited by
varying the illumination of individual ocelli (Stange
and Howard 1979). The only measurements of L-
neurone angular sensitivity reported to date are by
Wilson (1978 a), who measured this for median ocellar
neurones in the horizontal plane. Measurement of
the angular sensitivities of lateral ocellar L-neurones
in the vertical plane might show that individual L-
neurones have different receptive fields. For L4 and
L5, however, it is possible that any effect of a re-
stricted projection to the ocellar retina would be over-
come by the excitatory connexions they receive from
other L-neurones.
Recently Taylor (1981 a) has suggested that L-neu-
rones of the lateral ocelli can inhibit the responsive-
ness to illumination of some median ocellar L-neu-
rones. His evidence for this was that sometimes the
hyperpolarising response of a median L-neurone to
increased illumination was decreased if light was di-
rected at one of the lateral ocelli. Such an effect could
not be mediated by the type of connexion between
L-neurones which is described here. It is possible that
L-neurones of the median ocellus make different types
of connexion from those made by lateral L-neurones,
but no sign of such connexions have been seen in
the present study, although several recordings have
been made from L-neurones which connect the medi-
an and lateral ocelli (ML neurones) in conjunction
with pure median L-neurones. The possibility that
the effects reported by Taylor are mediated by small
second-order ocellar neurones, or by neurones driven
by the compound eyes cannot presently be ruled out.
The excitatory connexions between L-neurones
could clearly sharpen responsiveness to decreased
light intensity. This sharpening would be apparent
in the postsynaptic L-neurones and in third-order
ocellar neurones such as 03, which probably plays
a role in stabilising flight by monitoring movements
of the visual horizon (Simmons 1980). L-neurones
413
also boost the responsiveness of brain neurones to
stimulation of the compound eyes (Simmons 1981 a),
and a sharpening of response to decreased illumina-
tion would also be important here.
Inhibitory connexions among arrays of similar
visual neurones can enhance contrasts in the visual
field (Hartline et al. 1956). In the case of L-neurones,
however, the rapid decrement of the IPSPs would
make such enhancement short-lived. The inhibitory
connexions may help to enhance responsiveness to
a moving shadow. Imagine that two L-neurones,
which are connected by inhibitory connexions, have
different receptive fields, and that a shadow passes
first over the receptive field of one neurone and then
over that of the second. If the change in light intensity
is sufficient, the first L-neurone will spike. This will
cause an IPSP in the second L-neurone. The hyperpo-
larisation that this IPSP causes will enhance the abili-
ty of the second L-neurone to spike (Fig. 1), increas-
ing the amplitude of the spike it produces when the
shadow falls over its receptive field. The enhancement
will, of course, be short-lived, and most effective for
shadows which pass over the second L-neurone's re-
ceptive field about 5 ms after they pass over the first
(Figs. 3A, 4A, C, D). In addition,, the enhancement
will wane rapidly if a succession of shadows pass
in front of the ocellus, as might happen if a locust
were to fly beneath branches of a tree for example.
Similar connexions to the inhibitory ones made
between L-neurones might be found in movement-
detecting circuits of other eyes. A number of models
for these have been proposed (e.g. Reichardt 1962;
Barlow and Levick 1965), and they employ lateral
inhibition and elements with temporal filtering prop-
erties. They are difficult to test in the vertebrate or
compound eye retinas, however, because of the diffi-
culty in recording from two or more interconnected
neurones at the same time. In the compound eye
of the fly, there have been a number of ultrastructural
studies in which synapses made between some of the
larger second-order neurones have been examined
(e.g. Braitenberg and Debbage 1974; Strausfeld and
Campos-Ortega 1973; the literature to 1980 is re-
viewed by Shaw 1981).
Acknowedgements. I am grateful to Malcolm Burrows for advice
and encouragement. Some equipment was bought with a grant
from The Royal Society.
References
Autrum H, Zettler F, Jfirvilehto M (1970) Postsynaptic potentials
from a single monopolar neuron of the ganglion opticum 1
of the blowfly Calliphora. Z Vergl Physiol 70:414M24
Bacon J, Altman J (1977) A silver intensification method for cobalt-
filled neurones in wholemount preparations. 'Brain Res
138 : 359-363
414 P.J. Simmons: Connexions Between Second-Order Ocellar Neurones of Locusts
Barlow HB, Levick WR (1965) The mechanism of directionally
sensitive units in rabbit's retina. J Physiol (Lond) 178:477-
504
Blight AR, Llin/ts R (1980) The non-impulsive stretch receptor
of the crab: a study of depolarisation-release coupling at a
tonic sensorimotor synapse. Philos Trans Soc (Lond) [Biol]
290 : 219-276
Braitenberg V, Debbage P (1974) A regular net of reciprocal syn-
apses in the visual system of the fly Musca domestica. J Comp
Physiol 90 : 25-31
Burrows M, Siegler MVS (1978) Graded synaptic transmission
between local interneurones and motoneurones in the metatho-
racic ganglion of the locust. J Physiol (Lond) 285:231 255
Chappell RL, Dowling JE (1972) Neural organization of the medi-
an ocellus of the dragonfly. 1. Intracellular electrical activity.
J Gen Physiol 60:121-147
Dowting JE, Chappell RL (1972) Neural organization of the medi-
an ocellus of the dragonfly. 2. Synaptic structure. J Gen Physiol
60 : 148-165
Elmqvist D, Quastel DMJ (1965) A quantitative study of end-plate
potentials in isolated human muscle. J Physiol (Lond)
178 : 505-529
Goodman CS (1974) Anatomy of locust ocellar interneurons: con-
stancy and variability. J Comp Physiol 95:185-201
Goodman CS (1976) Anatomy of the ocellar interneurones of acri-
did grasshoppers. 1. The large interneurones. Cell Tissue Res
175 : 203325
Goodman CS (1978) Isogenic grasshoppers: genetic variability in
the morphology of identified neurons. J Comp Neurol
182 : 681-706
Goodman LJ, Mobbs PG, Guy R G (1977) Information processing
along the course of a visual interneuron. Experientia 33 : 748-750
Goodman LJ, Mobbs PG, Kirkham BJ (1979) The fine structure
of the ocellus of Schistocerca gregaria. The neural organization
of the synaptic piexus. Cell Tissue Res 196:487-510
Graubard K (1978) Synaptic transmission without action poten-
tials: input-output properties of a non-spiking presynaptic neu-
ron. J NeurophysioI 41 : 1014-1025
Guy RG, Goodman LJ, Mobbs PG (1979) Visual interneurons
in the bee brain: synaptic organization and transmission by
graded potentials. J Comp Physiol 134:253364
Hartline HK, Wagner HG, Ratliff F (1956) Inhibition in the eye
of Limulus. J Gen Physiol 39:651~673
Hengstenberg R (1977) Spike responses of "non-spiking" visual
interneurone. Nature 270:338 340
Katz B, Miledi R (1967) A study of synapfic transmission in the
absence of nerve impulses. J Physiol (Lond) 192:406426
Katz B, Miledi R (1971) The effect of prolonged depolarisation
on synaptic transfer in the stellate ganglion of the squid. J
Physiol (Lond) 216:503-512
Katz B, Thesleff S (1957) A study of the "desensitization" pro-
duced by acetyl-choline at the motor end-plate. J Physiol (Lond)
138:63-80
Kusano K, Landau EM (1975) Depression and recovery of trans-
mission at the squid giant synapse. J Physiol (Lond) 245:13-32
Laughlin SB (1973) Neural integration in the first optic neuropile
of dragonflies. 1. Signal amplification in dark-adapted second-
order neurons. J Comp Physiol 84 : 333-335
Laughlin SB, Hardie RC (1978) Common strategies for light adap-
tation in the peripheral visual systems of fly and dragonfly.
J Comp Physiol 128 : 319-340
Maynard DM, Walton KD (1975) Effects of maintained depolar-
ization of presynaptic neurons on inhibitory transmission in
lobster neuropil. J Comp Physiol 97 : 215-243
Miller RF (1979) The neuronal basis of ganglion-cell receptive
field organization and the physiology of amacrine cells. In:
Schmitt FO, Worden F G (eds) The neurosciences, Fourth study
program. MIT Press, Cambridge, Massachusetts
Mirolli M (1981) Fast inward and outward current channels in
a non-spiking neurone. Nature 292:251-253
Patterson JA, Goodman LJ (1974) Intracellular responses of recep-
tor cells and second order cells of the ocelli of the locust Schisto-
cerca gregaria. J Comp Physiol 95:237-250
Pearson KG, Goodman CS (1979) Correlation of variability in
structure with variability in synapfic connections of an identi-
fied interneuron in locusts. J Comp Neurol 184:141-166
Quicke DLJ, Brace RC (1979) Differentia1 staining of cobalt and
nickel-filled neurones using rubeanic acid. J Microsc
119:161-163
Reichardt W (1962) Nervous integration in the facet eye. Biophys
J 2:121-143
Shaw SR (1968) The organisation of the locust retina. Syrup Soc
Zool (Lond) 23:135-163
Shaw SR (1981) Anatomy and physiology of identified non-spiking
cells in the photoreceptor-lamina complex of the compound eye
of insects, especially Diptera. In: Roberts A, Bush BMH (eds)
Neurones without impulses. Cambridge University Press, Cam-
bridge
Siegler MVS, Burrows M (1979) The morphology of local non-
spiking interneurones in the metathoracic ganglion of the locust.
J Comp Neurol 183 : 121-148
Simmons PJ (1980) A locust wind and ocellar brain neurone. J
Exp Biol 85:281-294
Simmons PJ (1981 a) Ocellar excitation of the DCMD: an identified
locust interneurone. J Exp Biol 91:355-359
Simmons PJ (1981b) Synaptic transmission between second- and
third-order neurones of a locust ocellus. J Comp Physiol
145 : 265376
Stange G (1981) The ocellar component of equilibrium control
in dragonflies. J Comp Physiol 141:335-347
Stange G, Howard J (1979) An ocellar dorsal light response in
a dragonfly. J Exp Biol 83:351-355
Strausfeld NJ, Campos-Ortega JA (1973) The L4 monopolar neu-
rone: a substrate for lateral inhibition in the fly Musca domes-
tica (L.). Brain Res 59:97-117
Taylor CP (1981 a) Graded interactions between identified neurons
from the simple eyes of an insect. Brain Res 215:382-387
Taylor CP (1981b) Contributions of compound eyes and oceili
to steering of locusts in flight. 2. Timing changes flight motor
units. J Exp Biol 93 : 19-37
Werblin FS, Dowling JE (t969) Organization of the retina of the
mudpuppy Necturus maculosus: 2. Intracellular recording. J
Neurophysiol 32:339-355
Wilson M (1978a) The functional organisation of locust ocelli.
J Comp Physiol 124:297-316
Wilson M (1978b) Generation of graded potential signals in the
second order cells of locust ocellus. J Comp Physiol
124:317 331